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Diversity-oriented Enzymatic Modular Assembly of ABO Histo-blood Group Antigens Jinfeng Ye, Xian-wei Liu, Peng Peng, Wen Yi, Xi Chen, Fengshan Wang, and Hongzhi Cao ACS Catal., Just Accepted Manuscript • DOI: 10.1021/acscatal.6b02755 • Publication Date (Web): 01 Nov 2016 Downloaded from http://pubs.acs.org on November 1, 2016
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ACS Catalysis
Diversity-oriented Enzymatic Modular Assembly of ABO Histo-blood Group Antigens †, ∆
Jinfeng Ye,
†, ∆
Xian-wei Liu,
†
‡
§
Peng Peng, Wen Yi, Xi Chen, Fengshan Wang,
†,⊥
Hongzhi Cao*
,†, #
†
National Glycoengineering Research Center, Shandong Provincial Key Laboratory of Carbohydrate Chemistry and Glycobiology, Shandong University, Jinan 250100, China
‡
Institute of Biochemistry, College of Life Science, Zhejiang University, Hangzhou 310058, China
§
Department of Chemistry, University of California, One Shields Avenue, Davis, CA 95616, USA
⊥
Key Laboratory of Chemical Biology, Ministry of Education, School of Pharmaceutical Sciences, Shandong University, Jinan 250012, China #
State Key Laboratory of Microbiology, Shandong University, Jinan 250100, China.
KEYWORDS: biocatalysis, enzymatic synthesis, blood group, ABH antigen, diversity-oriented synthesis, glycosyltransferase
ABSTRACT: Enzymatic synthesis of all 15 naturally occurring human ABH antigens was achieved using a diversityoriented enzymatic modular assembly (EMA) strategy. Three enzyme modules were developed, each one-pot multienzyme module comprises a glycosyltransferase and one or two corresponding sugar nucleotide generating enzyme(s). These multienzyme cascade processes provide an efficient and convenient platform for collective synthesis of all 15 ABH antigens in three operationally simple steps from 5 readily available disaccharide acceptors and 3 simple free sugars as donor precursors. HO HO EMA Module 2
HO
OH O
O
HO OR'
OH
five disaccharide acceptors
O HO
OH O
OR'
O O HO
OR'
OH
OH
five A antigens
O
EMA Module 1
O HO AcHN O
OH
HO HO
OH
OH
HO
OH
HO
five H antigens EMA Module 3
OH O
OH
HO
O
HO O
OR'
O O HO
OH
OH
five B antigens
ABO blood group system is the major human alloantigen system that was initially discovered in 1901 by Karl Landsteiner, a winner of 1930 Nobel Prize in Physiology or Medicine.1 It is determined by expression of A, B, or H antigens as the terminal carbohydrate epitopes of glycoproteins and glycolipids on the red blood cells. There are approximate 2 million ABH glycan antigen sites on each red blood cell. These glycan antigens are responsible for the acute immune response of hemolytic transfusion reaction (HTR), bone marrow and organ transplantation.2 The ABH antigens are not confined to red blood cells but are also widely distributed on epithelial and endothelial cells of all organs, on neurons of the peripheral nervous system and secretion fluids such as human milk, saliva and urine.3 Accumulating evidences have demonstrat-
ed that these glycan antigens play pivotal and direct roles by serving as receptors for various bacterial, viral and parasite infections, and cancer metastasis.2,4,5 The structures of ABH antigen determinants comprising three carbohydrate epitopes were elucidated by Morgan and Watkins in 1957 (1−3, Figure 1a).6 Depending on different disaccharide precursors 4−8 (Figure 1b) in their biosynthetic pathway, the ABH antigens can be further divided into five subtypes with a total of 15 naturally occurring structures (Table 1).2,7 The structure diversity of ABH antigens is associated to the distinct susceptibility of human individuals to various pathogen infections as an evolutionary result of human ABO polymorphism. However, the molecular function of ABH antigens and the
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such as chemical synthesis,11-23 chemoenzymatic synthesis,24 enzymatic synthesis25-33 and whole-cell fermentation34. Despite numerous synthetic approaches reported so far, the collective synthesis of all 15 naturally occurring ABH antigens has only been achieved through elegant chemical synthesis by Lowary and co-workers recently.16-18 The non-natural Type V ABH antigens were also chemically synthesized by the Lowary group.18
driving force of these evolutionary process remain largely unknown.8,9 The biological significance and clinical importance of ABH antigens have ensured that their synthesis continues to be of significant interest for decades since the pioneering studies accomplished by Lemieux and co-workers in 1970s.10 In the new millennium, many different approaches have been explored for the synthesis of ABH antigens,
Figure 1. a) Structures of the A, B and H antigen determinants; b) Structure of the disaccharide precursors. R = glycoprotein, glycolipid or carbohydrate (R = R' in Scheme 1 and Table 1−4 for 4−8 which are used as acceptors in synthesis). Table 1. Synthetic targets of all 15 histo-blood group A, B and H antigens. Type I β β3
Type II
β3
α2
β
α2
9
β β3
A antigens
α
R' β4
H antigens
α2
D-Glucose (Glc)
α2
14
β
α3
α2
α2
α
19
α2
N-Acetyl-D-glucosamine (GlcNAc)
β3
β
R'
α3
17
β R'
β3
α2
β
α3
20
D -Galactose (Gal)
α3 α2
α2
21
N-Acetyl-D-galactosamine (GalNAc)
R'
18
R'
β4
R'
As an alternative approach, the glycosyltransferasebased multienzyme system provides a straightforward method to access complex glycans without tedious protecting group manipulation.35-41 Herein we describe a highly efficient enzymatic modular assembly (EMA) strategy for diversity-oriented parallel synthesis of all 15 naturally occurring ABH antigens 9−23 (Scheme 1).
α2
R'
13
12
16
β3
β
α2
β R'
α3
R'
α3
R'
β4 R'
15
β4
Type VI
β4
α2
11
α
α3
β
α3
β3
R'
α2
β
R'
β3
β3
B antigens
Type IV
R'
10
β4
α3
Type III
α3
22
L -Fucose (Fuc)
α2
R' =
β
R'
23
O
N3
As depicted in Scheme 1, the EMA module 1 is an onepot two-enzyme system which was designed for α1−2fucosylation of five readily available disaccharide acceptors 4−8 (Type I−IV and VI core structures) to provide five H antigens 9−13. The H antigens 9−13 serve as acceptors for subsequent α1−3-N-acetyl-galactosaminylation in EMA module 2 or for α1−3-galactosylation in EMA module 3 to produce five A antigens 14−18 or five B antigens
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ACS Catalysis tion using free monosaccharides (Fuc, GalNAc or Gal) as donor precursors. The Type I−IV and VI disaccharide acceptors 4−8 are readily available on large scale through chemoenzymatic synthesis or chemical synthesis as we reported previously.42-44
19−23, respectively. Each EMA module contains a glycosyltransferase and enzyme(s) for in situ generation of the corresponding sugar nucleotide donor (GDP-Fuc, UDPGalNAc, or UDP-Gal). This represents an operationally simple method for sequential one-pot sugar chain elonga-
OH
HO
OR'
ATP GTP
OH
disaccharides (4-8) HO
ADP PPi O
OH
BfFKP
HO
L-Fuc
EMA Module 1
O
HO
OH OH
O
OH
HO
EMA Module 1: α1_2-fucosylation
O
HO
OGDP OH
OH
4-8
OH
HO
OR'
OH
O
HO
OR'
O O
α1_2-FucT
GDP-Fuc
GDP
HO
OH
OH
9-13 EMA Module 2: α1_3-N-acetyl-galactosaminylation
OH
HO
O
HO
OH
HO
O
HO
OR'
O HO
OH
ATP UTP
OH
HO
H antigens (9-13)
O
HO
ADP PPi
OH
AcHN
OH
HO
AcHN OUDP
HO
OH O
HO OH
HO
HO
O
AcHN O
OR'
OH O
O
α1_3-GalNAcT
O O HO
OH
A antigens (14-18)
OR'
O O
OH HO
OH
O
HO
OH
HO
B antigens (19-23)
ATP UTP
OH
HO
D-Gal
UDP
HO
ADP PPi
14-18
O
HO
OH
HO
EcGalK/BLUSP
OR'
HO
O
HO
OH
HO
HO
OH O
UDP-Gal
OH
HO
O
HO O
OH
OH
OR'
O
9-13
O HO OUDP
OH
OH
OH
O
O
OR'
O
UDP-GalNAc
EMA Module 3: α1_3-galactosylation
HO O
O
9-13
OH
HO
OH
HO
O
HO
BlNahK/EcGlmU
D-GalNAc
EMA Module 3
HO
O
AcHN O
OH
OH
HO
HO
OH
HO HO
O OH
EMA Module 2
OR'
O
O
O
α1_3-GalT UDP
HO
OH
OH
19-23
Scheme 1. Retrosynthetic plan for diversity-oriented enzymatic modular assembly of all 15 ABH antigens (9-23).
It is challenging to find a suitable α1−2fucosyltransferase (α1−2-FucT) which can use all five distinct disaccharide acceptors 4−8 for EMA module 1 (Scheme 1) for systematic synthesis of all five H antigens 9−13. FUT1 and FUT2 are two α1−2-FucTs which are responsible for in vivo biosynthesis of H antigens in mammalian system. Unfortunately, neither has been reported to be functionally expressed in Escherichia coli.2,34 On the other hand, a few bacterial α1−2-FucTs have been cloned and overexpressed as recombinant enzymes in Escherichia coli.28-30, 45-48 Most of them, however, are restricted to use β1−3-linked galactosides as acceptors except for WbgL30 from Escherichia coli O126 which prefers β1−4linked galactosides as acceptors. After substrate specificity screening, we are delighted to find that FutC25 from Helicobacter pylori can recognize all three β1−3-linked galactosides 4, 6 and 7, while WbgL can utilize the remaining two β1−4-linked galactosides 5 and 8. Therefore, FutC and WbgL were chosen as complementary α1−2FucTs in EMA module 1 for the synthesis of the desired H antigens. In this one-pot two-enzyme α1−2-fucosylation process, a bifunctional L-fucokinase/GDP-fucose pyrophosphorylase from Bacteroides fragilis (BfFKP)49 was responsible for converting L-fucose to GDP-fucose in the presence of adenosine 5'-triphosphate (ATP, 1.5 equiv.), guanosine 5'triphosphate (GTP, 1.5 equiv.), and MnCl2 (10 mM) in Tris-HCl buffer (100 mM, pH 7.5). The in situ generated GDP-fucose was then used by a recombinant FutC to
form H Type I antigen 9, Type III antigen 11, and Type IV antigen 12 (Scheme 1 and Table 2). FutC was replaced by WbgL in EMA module 1 for the synthesis of H Type II antigen 10 and Type VI antigen 13. The FutC-catalyzed α1−2-fucosylation reactions were completed in 4 hours at 37 °C for disaccharide acceptors 4, 6 and 7 with up to 80% yields, while the WbgL-catalyzed α1−2-fucosylation of disaccharide acceptors 5 and 8 required a longer incubation (36 hours) and moderate yields were achieved. The low yields of WbgL-catalyzed α1−2-fucosylation were consistent with its previously reported activity for Type II and Type VI disaccharides with an aglycon.30 All five H antigen 9−13 were obtained in this one-pot single operation step on preparative scales (66−277 mg, see ESI for details) after purification (Table 2). The purified H antigens 9−13 were used as acceptors in EMA module 2 for one-pot three-enzyme parallel synthesis of A antigens 14−18 (Scheme 1). In this module, Nacetyl-galactosamine (GalNAc) was activated to form UDP-GalNAc in the presence of ATP (1.2 equiv.), uridine 5'-triphosphate (UTP, 1.2 equiv.), MgCl2 (20 mM), and a fusion enzyme BlNahK-EcGlmU50 constructed from Bifidobacterium longum N-acetylhexosamine-1-kinase (BlNahK) and Escherichia coli N-acetylglucosamine uridyltransferase (EcGlmU) in Tris-HCl buffer (100 mM, pH 8.0). The in situ generated UDP-GalNAc was then utilized as a donor by a Helicobacter mustelae α1−3-N-acetylgalactosaminyltransferase (BgtA)27 to form A antigens 14−18, respectively. All five H antigens 9−13 are well toler-
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ated in EMA module 2 to produce A antigens 14−18 in one-pot on preparative scales in up to 90% yields after purification (Table 3).
Table 3. Enzymatic modular assembly of A antigens 14-18.
Entry
Acceptor
β
β
1
β3
R'
4
β
2
80 9
β4
5
1
α2
β
3
β3
10
β
α
4
β3
7
β4
β
5
α2
8
4
13
α2
R'
95
15
α
R'
R'
β3
90 α2
16
β
R'
R'
β3
94
α3
α2
12
β4
5
β
β
17
R'
12
β4
β4 α3
α3
β3
89
R'
95 14
R'
11
β3
α2
R'
11
β
β
R'
α2
α2
β3
95 α2
β
α2
3
β3
6
α3
9
R'
72
α
R'
R'
β3
β4
2
α2
α
β
R'
10
R'
α2
β3
Yield (%)
Product
R'
β3
α2
β4
Yield (%)
Product
Acceptor β
Table 2. Enzymatic modular assembly of H antigens 9-13.
Entry
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α2
β
β4
R' α3
α2
13
β
R'
92
18
R'
49
Table 4. Enzymatic modular assembly of B antigens 1923.
Entry The key for our designed EMA module 3 is to find a suitable α1−3-galactosyltransferase (α1−3-GalT) as shown in Scheme 1. Among a limited list of candidates, human blood group B glycosyltransferase (GTB) is an α1−3-GalT for in vivo biosynthesis of human ABO blood group B antigens from H antigens. Human GTB has been successfully overexpressed in Escherichia coli. However its substrate specificity towards 5 different types of H antigens is still unknown.51 On the other hand, a bacterial α1−3-GalT from Escherichia coli O86 (WbnI)28 was shown capable of using a Type III H antigen as the acceptor for the synthesis of the corresponding B antigen. The substrate specificity screening for WbnI using UDP-Gal as the donor indicates that WbnI can only tolerate Type I, Type III, and Type IV H antigens 9, 11−12 for producing B antigens 19 and 21−22 in less than 50% yields. The yields dropped significantly when in situ generated UDP-Gal was used. Unexpectedly, the recombinant human GTB51 could tolerate all five H antigens 9−13 as acceptors in our substrate specificity screening, and provides all five B antigens 19−23 in satisfied yields either using UDP-Gal directly as the donor or using in situ generated UDP-Gal as the donor. These results indicate that GTB is a superb α1−3-GalT for EMA module 3.
Acceptor β β3
1
α2
β
R'
α3
9
β
R'
α2
α2
β4 α2
α β3
β
α2
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60 β
R'
α3
12
β
13
R'
α2
α2
R'
98 22
β4 α3
R'
21
β3
β4
5
95 α
11
β3
R'
20
β3 α3
α2
β
R'
3
4
90 19
α3
10
α2
R'
β3
β4
2
Yield (%)
Product
β
23
R'
97
4
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In this one-pot three-enzyme module, galactose was first converted to galactose-1-phosphate (Gal-1-P) by Escherichia coli galactokinase (EcGalK)52 in Tris-HCl buffer (100 mM, pH 7.5) in the presence of ATP (1.2 equiv) and MgCl2 (20 mM). The resulting Gal-1-P was utilized by a Bifidobacterium longum UDP-sugar pyrophosphorylase (BLUSP)53 in the presence of UTP (1.2 equiv) to form UDP-Gal, and this in situ generated UDP-Gal was used by GTB as a donor to provide the desired B antigens 19−23 in good yields except for acceptor 11 which was resulted with only a 60% yield (Table 4). These results indicate that GTB has promiscuous substrate specificity towards all 5 natural H antigens as acceptors. More interestingly, the glycosidic bond conformation at the reducing end of disaccharide acceptor can dramatically affect the GTBcatalyzed glycosylation outcome as the yield for 21 is much lower than 22. In summary, systematic enzymatic synthesis of all 15 naturally occurring histo-blood group ABH antigens was achieved by using an enzymatic modular assembly (EMA) strategy. This new strategy provides an operationally simple and elegant access for diversity-oriented parallel synthesis of all 15 ABH antigens in only three steps from 5 readily available disaccharide acceptors and 3 monosaccharides as donor precursors. This EMA strategy is also amenable for the parallel synthesis of other focused complex glycan libraries.
ASSOCIATED CONTENT Supporting Information. The supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acscatal.xxxxxxx. Materials and methods, synthetic procedures, characterization of products, and NMR spectra (PDF)
AUTHOR INFORMATION Corresponding Author * E-mail:
[email protected] Author Contributions ∆
J.Y. and X.L. contributed equally to this work.
Notes The authors declare no competing financial interest.
ACKNOWLEDGMENT We are grateful to Prof. Peng George Wang of Georgia State University for BgtA and WbnI plasmids. This work was financially supported by the Major State Basic Research Development Program of China (973 Program, No. 2012CB822102), National Natural Science Foundation of China (Grant Nos. 21372145, 21672128) and State Key Laboratory of Microbial Technology (M2016-06).
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